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Accuracy of Mandibular Force Profiles for Bite Force Estimation and Feeding

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Accuracy of Mandibular Force Profiles for Bite Force Estimation and Feeding © 2016. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2016) 219, 3738-3749 doi:10.1242/jeb.143339 RESEARCH ARTICLE Accuracy of mandibular force profiles for bite force estimation and feeding behavior reconstruction in extant and extinct carnivorans François Therrien1,2,*, Annie Quinney2, Kohei Tanaka2 and Darla K. Zelenitsky2 ABSTRACT processing food. Various biomechanical approaches have been Mandibular force profiles apply the principles of beam theory to developed to investigate and compare the feeding behaviors and bite identify mandibular biomechanical properties that reflect the bite capabilities of extant and extinct mammalian predators, such as force and feeding strategies of extant and extinct predators. While beam theory (e.g. Biknevicius and Ruff, 1992a; Therrien, 2005a,b; this method uses the external dimensions of the mandibular corpus to Organ et al., 2006), jaw musculature reconstructions (e.g. determine its biomechanical properties, more accurate results could Christiansen and Adolfssen, 2005; Wroe et al., 2005; Christiansen potentially be obtained by quantifying its internal cortical bone and Wroe, 2007), and finite-element analysis (FEA) (e.g. McHenry distribution. To test this possibility, mandibular force profiles were et al., 2007; Slater et al., 2009, 2010; Tseng and Binder, 2010; calculated using both external mandibular dimensions (‘solid Tseng and Wang, 2010; Tseng et al., 2011; Jones et al., 2013; mandible model’) and quantification of internal bone distribution of Tseng, 2013; Wroe et al., 2013; Figueirido et al., 2014). Although the mandibular corpus obtained from computed tomography scans most methods require exquisitely preserved specimens (i.e. (‘hollow mandible model’) for five carnivorans (Canis lupus, Crocuta complete or undistorted specimens) and/or extensive crocuta, Panthera leo, Neofelis nebulosa and the extinct Canis dirus). computational facilities [i.e. access to computed tomography (CT) Comparison reveals that the solid model slightly overestimates scanners and bioengineering software], the mandibular force profile mandibular biomechanical properties, but the pattern of change in method is simpler and has the advantages of being easily biomechanical properties along the mandible remains the same. As reproducible, widely applicable to various taxa and requiring only such, feeding behavior reconstructions are consistent between the access to isolated mandibles (e.g. Therrien, 2005a,b; Therrien et al., two models and are not improved by computed tomography. Bite 2005; Christiansen, 2007; Blanco et al., 2011; Jasinski, 2011). force estimates produced by the two models are similar, except in C. Mandibular force profiles apply beam theory to determine the crocuta, where the solid model underestimates bite force by 10–14%. biomechanical properties of mandibles, which reflect the loads and This discrepancy is due to the more solid nature of the C. crocuta stresses endured by mandibles during life (Biknevicius and Ruff, mandible relative to other carnivorans. Therefore, computed 1992a; Therrien, 2005a,b; Therrien et al., 2005). This approach tomography improves bite force estimation accuracy for taxa with follows the assumption that bone has evolved to achieve maximum thicker mandibular corpora, but not significantly so otherwise. Bite strength with a minimum amount of material and to remodel itself in force estimates derived from mandibular force profiles are far closer to response to the loads to which it is subjected. Reflecting this notion, empirically measured bite force than those inferred from jaw both cortical thickness and bone shape will reflect the habitual loads musculature dimension. Consequently, bite force estimates derived experienced during life: elliptical shapes characterize bones that from this method can be used to calibrate finite-element analysis undergo higher bending stresses in one direction over another models. whereas greater cortical thickness characterizes bones subjected to high loads (see Wainwright et al., 1982; Lanyon and Rubin, 1985). KEY WORDS: Beam theory, Mandible, Feeding behavior, Bite force, Mandibular force profiles use the external dimensions of mandibles Carnivora, Computed tomography to model them as solid, elliptical beams composed of cortical bone that undergo bending loads during ingestion, here termed the ‘solid INTRODUCTION mandible model’ (Fig. 1; equivalent to the ‘solid symmetrical Feeding behavior and bite force are significant aspects of the model’ of Biknevicius and Ruff, 1992b). However, mandibles ecology of a predator, as both play an important role in determining modeled as solid ellipses may poorly reflect the mandible capacity the type and/or size of prey hunted and the trophic position of the to withstand bending stresses for three reasons: (1) the mandibular predator (Meers, 2002; Verwaijen et al., 2002; Wroe et al., 2005; corpus contains porous cancellous bone, thus making it partly Van Valkenburgh, 2007; see also Wiersma, 2001). Feeding hollow, (2) the amount of cancellous bone in the mandibular cross- behavior in extinct predators is usually inferred from the study of section varies along the mandible and between taxa, and (3) the their craniomandibular characteristics and dental morphology, cross-section of a mandible may differ from a perfect elliptical shape which can be interpreted as adaptations for capturing prey and (see Biknevicius and Ruff, 1992b). As such, these divergences could lead to erroneous estimation of the biomechanical properties of the mandible, resulting in the misinterpretation of feeding 1Royal Tyrrell Museum of Palaeontology, PO Box 7500, Drumheller, Alberta, behavior and bite force. Canada T0J 0Y0. 2Department of Geoscience, University of Calgary, 2500 University Drive NW, Calgary, Alberta, Canada T2N 1N4. More accurate determination of mandibular biomechanical properties can potentially be achieved by quantifying the amount *Author for correspondence ([email protected]) and distribution of cortical bone in the cross-section of the F.T., 0000-0002-2652-908X mandibular corpus through the use of X-ray imagery and CT scans (Biknevicius and Ruff, 1992b). To investigate the impact of Received 23 May 2016; Accepted 8 September 2016 X-ray imagery on the accuracy of mandibular force profiles, Journal of Experimental Biology 3738 RESEARCH ARTICLE Journal of Experimental Biology (2016) 219, 3738-3749 doi:10.1242/jeb.143339 scanner (slice thickness 1 mm, pixel dimension 0.2 mm, energy List of symbols and abbreviations and current levels were not recorded but presumably close to the CA cortical bone area in mandibular cross-section standards of 120 kV and 200 mA; see Ridgely and Witmer, 2006) FEA finite-element analysis in the Department of Anthropology at the National Museum of Ix second moment of area about the mediolateral axis Natural History, Washington, DC, USA. The ramus was oriented in Iy second moment of area about the dorsoventral axis life position and CT scans were selectively made at each individual M first molar (carnassial) 1 interdental gap in the coronal plane, perpendicular to the neutral M2 second molar M3 third molar axis (which is approximated by the central axis) of the mandible P2 second premolar (Fig. 2). At the canine, CT scans were taken diagonally from the P3 third premolar lingual aspect of the symphysis through the posterior margin of P4 fourth premolar the canine alveolus so the CT slices were taken perpendicular to the TA total area of mandibular cross-section neutral axis of the mandible. The distance between each interdental USNM United States National Museum of Natural History, L Smithsonian Institution, Washington, DC gap and the middle of the articular condyle ( ) was measured with Zx section modulus about the mediolateral axis calipers. Zx/L dorsoventral mandibular force Individual CT slices were saved as IMA files and analyzed using Zx/Zy relative mandibular force (or overall mandibular shape) the software ImageJ v. 1.40g (National Institutes of Health, Zy section modulus about the dorsoventral axis Bethesda, MD, USA). Mandibular depth and width, defined as the greatest diameter of the mandibular corpus in the vertical and horizontal planes, respectively, were measured on each CT slice mandibles of extant and extinct carnivorans were CT scanned to with the ImageJ measuring tool (Fig. 1). A few CT slices were quantify the internal distribution of cortical bone in the mandibular edited in ImageJ to better define the extent of cortical bone (with corpus in order to derive revised mandibular force profiles, an white paintbrush tool), erase cancellous bone and tooth crowns approach here termed the ‘hollow mandible model’ (Fig. 1). These (with black paintbrush tool), and fill tooth alveoli for analytical results were compared with mandibular force profiles derived from purposes (with white paintbrush tool). When the distinction external mandibular dimensions measured on the same CT data (i.e. between cortical bone and medullary cavity was difficult to ‘solid mandible model’) in order to determine: (1) whether feeding behavior interpretations differ between the two models, and (2) L whether the hollow mandible model provides more accurate bite force estimates than the solid mandible model. As such, this study will determine whether the use of CT significantly affects paleoecological interpretations based on mandibular force profiles derived from external measurements. MATERIALS AND METHODS Samples Dentaries of five carnivoran species [Panthera
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